The higher order auditory cortex is involved in the assignment of affective value to sensory stimuli

Nature Communications

Volumn 6, Issue , 2015, Pages

  Grosso, Anna ^a   Cambiaghi, Marco ^a   Renna, Annamaria ^a   Milano, Luisella ^a   Roberto Merlo, Giorgio ^a   Sacco, Tiziana ^a   Sacchetti, Benedetto ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b National Institute of Neuroscience INN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; NEUROLOGY; RODENT; SENSORY SYSTEM;

ACOUSTIC NERVE FIBER; AMNESIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; AUDITORY CORTEX; AUDITORY CORTEX TE2; BRAIN FUNCTION; CONTROLLED STUDY; FEAR; GENE SILENCING; INFORMATION RETRIEVAL; LATERAL AMYGDALA; MALE; MEMORY CONSOLIDATION; MOTOR PERFORMANCE; NEUROPATHOLOGY; NONHUMAN; PERSONAL EXPERIENCE; PHARMACOGENETICS; RAT; RECALL; SALIENCE NETWORK; SENSORY STIMULATION; SIGNAL TRANSDUCTION; ANIMAL; AUDITORY STIMULATION; EMOTION; HUMAN; MEMORY; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; WISTAR RAT;

RATTUS;

ACOUSTIC STIMULATION; AMNESIA; ANIMALS; AUDITORY CORTEX; EMOTIONS; FEAR; HUMANS; MALE; MEMORY; NEURONS; RATS; RATS, WISTAR;

EID: 84949293642     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9886     Document Type: Article

References (54)

1. LeDoux, J. E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23, 155-184 (2000).
2. Paton, J. J., Belova, M. A., Morrison, S. E. & Salzman, C. D. The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865-870 (2006).
3. Redondo, R. L. et al. Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 513, 426-430 (2014).
4. Salimpoor, V. N. et al. Interactions between the nucleus accumbens and auditory cortices predict music reward value. Science 340, 216-219 (2013).
5. Xiu, J. et al. Visualizing an emotional valence map in the limbic forebrain by TAI-FISH. Nat. Neurosci. 17, 1552-1559 (2014).
6. Duvarci, S. & Pare, D. Amygdala microcircuits controlling learned fear. Neuron 82, 966-980 (2014).
7. Ohl, F. W. & Scheich, H. Learning-induced plasticity in animal and human auditory cortex. Curr. Opin. Neurobiol. 15, 470-477 (2005).
8. Brosch, M., Selezneva, E. & Scheich, H. Representation of reward feedback in primate auditory cortex. Front. Syst. Neurosci. 5, 5 (2011).
9. Weinberger, N. M. New perspectives on the auditory cortex: learning and memory. Handb. Clin. Neurol. 129, 117-147 (2015).
10. Weinberger, N. M. Specific long-Term memory traces in primary auditory cortex. Nat. Rev. Neurosci. 5, 279-290 (2004).
11. Grosso, A., Cambiaghi, M., Concina, G., Sacco, T. & Sacchetti, B. Auditory cortex involvement in emotional learning and memory. Neuroscience 299, 45-55 (2015).
12. Sacco, T. & Sacchetti, B. Role of secondary sensory cortices in emotional memory storage and retrieval in rats. Science 329, 649-656 (2010).
13. Kolb, B. & Tees, R. C. The Cerebral Cortex of the Rat 99-101 and 381-392 (MIT Press, 1990).
14. Paxinos, G. The Rat Nervous System 1051-1063 (Academic Press Elsevier, 2004).
15. Romanski, L. M. & LeDoux, J. E. Information cascade from primary auditory cortex to the amygdala: corticocortical and corticoamygdaloid projections of temporal cortex in the rat. Cerebr. Cortex 3, 515-532 (1993).
16. Sacchetti, B., Lorenzini, C. A., Baldi, E., Tassoni, G. & Bucherelli, C. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J. Neurosci. 19, 9570-9578 (1999).
17. Lesburgueres, E. et al. Early tagging of cortical networks is required for the formation of enduring associative memory. Science 331, 924-928 (2011).
18. Martin, J. H. & Ghez, C. Pharmacological inactivation in the analysis of the central control of movement. J. Neurosci. Methods 86, 145-159 (1999).
19. Schneider, D. M. & Mooney, R. Motor-related signals in the auditory system for listening and learning. Curr. Opin. Neurobiol. 27, 78-84 (2015).
20. Zhou, M. et al. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat. Neurosci. 17, 841-850 (2014).
21. Remington, E. D., Osmanski, M. S. & Wang, X. An operant conditioning method for studying auditory behaviors in marmoset monkeys. PLoS ONE 7, e47895 (2012).
22. Xiong, Q., Znamenskiy, P. & Zador, A. M. Selective corticostriatal plasticity during acquisition of an auditory discrimination task. Nature 521, 348-351 (2015).
23. de Oca, B. M., Minor, T. R. & Fanselow, M. S. Brief flight to a familiar enclosure in response to a conditional stimulus in rats. J. Gen. Psychol. 134, 153-172 (2007).
24. Gewirtz, J. C. & Davis, M. Using pavlovian higher-order conditioning paradigms to investigate the neural substrates of emotional learning and memory. Learn. Mem. 7, 257-266 (2000).
25. Nader, K. & LeDoux, J. The dopaminergic modulation of fear: quinpirole impairs the recall of emotional memories in rats. Behav. Neurosci. 113, 152-165 (1999).
26. Rescorla, R. A. in Contemporary Approaches to Conditioning and Learning (eds McGuigan, F. J. & Lumsden, D. B.) 127-150 (Washington DC: V.H. Winston, 1973).
27. Anderson, A. K. et al. Dissociated neural representations of intensity and valence in human olfaction. Nat. Neurosci. 6, 196-202 (2003).
28. Russell, J. A. A circumplex model of affect. J. Personal. Soc. Psychol. 39, 1161-1178 (1980).
29. Reichelt, A. C. & Lee, J. L. Memory reconsolidation in aversive and appetitive settings. Front. Behav. Neurosci. 7, 118 (2013).
30. Pastalkova, E. et al. Storage of spatial information by the maintenance mechanism of LTP. Science 313, 1141-1144 (2006).
31. Kwapis, J. L. & Helmstetter, F. J. Does PKM(zeta) maintain memory? Brain Res. Bull 105, 36-45 (2014).
32. Guzowski, J. F. et al. Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr. Opin. Neurobiol. 15, 599-606 (2005).
33. Saddoris, M. P., Holland, P. C. & Gallagher, M. Associatively learned representations of taste outcomes activate taste-encoding neural ensembles in gustatory cortex. J. Neurosci. 29, 15386-15396 (2009).
34. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
35. Fanselow, M. S. Factors governing one-Trial contextual conditioning. Anim. Learn. Behav. 18, 264-270 (1990).
36. Sacchetti, B., Scelfo, B., Tempia, F. & Strata, P. Long-Term synaptic changes induced in the cerebellar cortex by fear conditioning. Neuron 42, 973-982 (2004).
37. Hatfield, T., Han, J. S., Conley, M., Gallagher, M. & Holland, P. Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J. Neurosci. 16, 5256-5265 (1996).
38. Koya, E. et al. Targeted disruption of cocaine-Activated nucleus accumbens neurons prevents context-specific sensitization. Nat. Neurosci. 12, 1069-1073 (2009).
39. Cruz, F. C., Javier Rubio, F. & Hope, B. T. Using c-fos to study neuronal ensembles in corticostriatal circuitry of addiction. Brain. Res. doi:10.1016/j.brainres (14) 2014.11.005 (2014).
40. Bao, S., Chan, V. T. & Merzenich, M. M. Cortical remodelling induced by activity of ventral tegmental dopamine neurons. Nature 412, 79-83 (2001).
41. Gonzalez-Lima, F. & Scheich, H. Ascending reticular activating system in the rat: a 2-deoxyglucose study. Brain Res. 344, 70-88 (1985).
42. Gonzalez-Lima, F., Finkenstadt, T. & Ewert, J. P. Learning-related activation in the auditory system of the rat produced by long-Term habituation: a 2-deoxyglucose study. Brain Res. 489, 67-79 (1989).
43. Wan, H. et al. Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds. Eur. J. Neurosci. 14, 118-124 (2001).
44. Kwon, J. T., Jhang, J., Kim, H. S., Lee, S. & Han, J. H. Brain region-specific activity patterns after recent or remote memory retrieval of auditory conditioned fear. Learn. Mem. 19, 487-494 (2012).
45. Pi, H. J. et al. Cortical interneurons that specialize in disinhibitory control. Nature 503, 521-524 (2013).
46. Schafe, G. E. & LeDoux, J. E. Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci. 20, RC96 (2000).
47. Letzkus, J. J. et al. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335 (2011).
48. David, S. V., Fritz, J. B. & Shamma, S. A. Task reward structure shapes rapid receptive field plasticity in auditory cortex. Proc. Natl Acad. Sci. USA 109, 2144-2149 (2012).
49. Yin, P., Fritz, J. B. & Shamma, S. A. Rapid spectrotemporal plasticity in primary auditory cortex during behavior. J. Neurosci. 34, 4396-4408 (2014).
50. Chavez, C. M., McGaugh, J. L. & Weinberger, N. M. The basolateral amygdala modulates specific sensory memory representations in the cerebral cortex. Neurobiol. Learn. Mem. 91, 382-392 (2009).
51. Chavez, C. M., McGaugh, J. L. & Weinberger, N. M. Activation of the basolateral amygdala induces long-Term enhancement of specific memory representations in the cerebral cortex. Neurobiol. Learn. Mem. 101, 8-18 (2013).
52. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Academic Press Elsevier, 1986).
53. Zilles, K. The Cortex of the Rat (Springer-Verlag, 1985).
54. Taubenfeld, S. M., Wiig, K. A., Bear, M. F. & Alberini, C. M. A molecular correlate of memory and amnesia in the hippocampus. Nat. Neurosci. 2, 309-310 (1999).